J. exp. Btol. 127, 389-400 (1987)
389
Printed m Great Britain © The Company of Biologists Limited 1987
INSTANTANEOUS OXYGEN CONSUMPTION AND
MUSCLE STROKE WORK IN MALACOSOMA AMERICANUM
DURING PRE-FLIGHT WARM-UP
By TIMOTHY M. CASEY AND JERI R. HEGEL-LITTLE
Department of Entomology and Economic Zoology, New Jersey Agricultural
Experiment Station, Cook College, Rutgers University, New Brunswick,
NJ 08903, USA and University of Medicine and Dentistry of New Jersey,
Rutgers Medical School, Piscataway, NJ 08854, USA
Accepted 19 August 1986
SUMMARY
Instantaneous rates of oxygen consumption (VOz), thoracic temperature (T th )
and wing stroke frequency (n) were continuously measured at several ambient
temperatures (T.) during pre-flight warm-up and subsequent cooling in a small
volume (30ml), open flow (240-300 ml min"1) respirometer. Heat production (HP)
was tightly coupled to T t h and independent of T.. The rate of change of HP
(mWmin" 1 ) was directly related to T a . Total cost of warm-up was strongly,
inversely related to T a . The energetic cost of cooling was a small fraction of the total
cost of warm-up. Increased energy expenditure occurred as a result of increases in
both n and stroke work input. The latter increased from 0-58 to 1*1 mj stroke"' at
low T ^ (13-25°C) and was essentially constant at higher T ^ (25-40°C). Wing
stroke frequency increased continuously and linearly with T t h . In contrast to
previous estimates based on heat exchange analyses, stroke work during warm-up
was equivalent to values measured during free hovering flight. These data are consistent with the hypothesis that energy expenditure is maximized during warm-up.
INTRODUCTION
In many insects, heat is produced by the flight muscles to elevate thoracic
temperature (T th ) prior to take-off (Dotterweigh, 1928; Krogh & Zeuthen, 1941).
Although all heat production occurs essentially in the flight muscles, their quantitative performance during warm-up has been difficult to evaluate. Estimates of the
metabolism per contraction of flight muscle of synchronous fliers during pre-flight
warm-up have been made based on measurements of heat storage and heat loss of the
thorax (Heinrich & Bartholomew, 1971; May, 1979; Casey, Hegel & Buser, 1981).
However, those studies underestimate total heat exchange because they do not
account for heat loss and heat storage from the head and the abdomen (Hegel &
Casey, 1982). Moreover, measured instantaneous rates of oxygen consumption (V o )
during warm-up significantly exceeded values obtained from calculations of heat
Key words: oxygen consumption, stroke work input, warm-up, energetics.
390
T. M. CASEY AND J. R.
HEGEL-LITTLE
exchange parameters (May, 1979; Bartholomew, Vleck & Vleck, 1981). However,
these authors did not report wing stroke frequency (n) and, therefore, important
details of muscle performance cannot be characterized from their data. Although the
role of T t h in determining stroke frequency is well known (Kammer & Heinrich,
1978; Kammer, 1981), metabolism during warm-up is dependent not only on
frequency of muscle contraction, but also on the energy expended per contraction
(stroke work input, E/n). The latter cannot be derived with sufficient precision
without simultaneous measurement of n, T th and V o .
The flight muscles serve different purposes in warm-up and flight. During warmup, the muscles raise Tth to the minimum temperature necessary for continuous
flight. This process has been postulated to occur as rapidly as possible to reduce the
time when the moth is grounded and vulnerable to predators (Bartholomew &
Heinrich, 1973; Heinrich & Casey, 1973). Thus, it should be advantageous for the
muscle to produce as much heat as possible (i.e. to operate at or near maximal rates).
During flight, the muscles supply the amount of lift appropriate to flight conditions.
Estimates of metabolism of moths during warm-up based on heat exchange calculations suggest that energy expenditure is lower during warm-up than during flight at
the same T t h (Heinrich, 1974; Casey et al. 1981; Heinrich & Mommsen, 1985). This
result is puzzling if the moths are warming up as rapidly as possible. In an attempt to
resolve this paradox we undertook to re-examine the energetics of pre-flight warm-up
in the tent caterpillar moth (Malacosoma americanum). The present study reports
instantaneous rates of VQ , Tth and muscle contraction frequency during pre-flight
warm-up. These data are used to determine energy expenditure throughout warmup, and to quantify the effects of muscle temperature on the energetics of muscle
contraction. We conducted our experiments at several T a values to examine the
effects of T a on the energetics of warm-up.
MATERIALS AND METHODS
Animals
Male moths were collected in the Hutcheson Memorial Forest (Somerset County,
New Jersey) in June 1982. Procedures for collection, storage and handling were
similar to those described in an earlier paper (Casey et al. 1981).
Oxygen consumption
Due to the rapidly changing rates of oxygen uptake during pre-flight warm-up (see
Bartholomew et al. 1981) experiments were conducted in a high flow (240-300 ml
min" 1 ), small volume respirometer. The chamber, a 35ml plastic, transparent,
Coulter-counter vial was connected to an Applied Electrochemistry Inc. Oxygen
Analyzer (S3A-sensor N22M) via a T-tube. A small opening was made in the lid of
the vial for thermocouples, impedance leads and incurrent air flow. An identical
chamber was attached to the other end of the T-tube. During experiments, the
empty chamber was clamped off with mosquito forceps. The fractional oxygeil
concentration of incurrent air (Fl o ) prior to and immediately following eacn
Energetics and muscle performance
391
experiment was determined by clamping off the animal respirometer and allowing
room air to flow through the empty chamber. Prior to gas analysis the air was dried
by passing it through a column of dessicant. The effective volume of the chamber
and rates of instantaneous oxygen consumption were determined by the method
described by Bartholomewet al. (1981). A respiratory quotient of 0-85 was assumed
(Joos, 1986). All gas volumes were converted to STPD. Heat production (HP) was
calculated from oxygen consumption data assuming that 1 ml O2 is equivalent to
201J.
Thoracic temperature
A small area of scales was removed from the dorsal thorax using microforceps. We
implanted 44-gauge copper-constantan thermocouples into the dorsal thorax after
punching a small hole in the cuticle with a microsurgical needle. During implantation the moth was placed in a plastic box filled with crushed ice. This treatment
kept thoracic temperature well below 10°C and made the use of anaesthesia unnecessary. Implanted wires were held in place by dried haemolymph and required no
further attention. The moths were usually allowed a quiescent period in the ice after
implantation (about 30min). They were then transferred to the appropriate thermal
regime. Since they were not anaesthetized, they often began typical pre-flight warmup behaviour immediately after T ^ had passively warmed to 10—15°C.
Thoracic and ambient temperature were monitored using alternate channels
of a two-channel Bailey Instruments Laboratory Thermometer whose output was
attached to another servo channel of the polygraph. This arrangement allowed us to
obtain continuous, simultaneous data for thoracic temperature and oxygen uptake.
Wing stroke frequency
Wing stroke frequency (n) was measured by implanting 44-gauge constantan wire
into two holes made in the dorsal thorax (see above) on either side of the dorsal
midline. The wires were attached to an impedance converter whose output was
recorded on a polygraph.
RESULTS
Thoracic temperature
During warm-up, Tth of Malacosoma americanum increased linearly with time at
rates which were strongly and linearly related to T a (Fig. 1). Correlation coefficients
for linear regressions of thoracic temperature versus time exceeded 0-99 at all T a
values. Mean rates of warm-up of 2-6°C min" 1 at T a of 13°C and 10°C min" 1 at T a of
25 °C were not significantly different from values predicted from regression analysis
of our previous data (Casey et al. 1981). Therefore, although the previous data were
llected in still air, it is apparent that airflow within the respirometer did not
arkedly affect rates of convective cooling and subsequent rates of warm-up.
K
392
T. M. CASEY AND J. R. HEGEL-LITTLE
14
12
JT- 10
o
o
oc
4
10
15
20
T (X).
25
30
Fig. 1. Rates of pre-flight warm-up in relation to ambient temperature for moths
warming inside the respirometer. Solid line indicates linear regression. Dashed line
represents the same relationship for moths warming up outside the respirometer in still
air (from Casey, Hegel & Buser, 1981).
Wing stroke frequency
The wing stroke frequency during warm-up was tightly coupled to thoracic
temperature, varying from 15 s" 1 at T t h = 15°C to about 55 s"1 at T t h = 35°C. The
temperature of the muscle rather than the ambient temperature determined the
frequency of muscle contraction. Slopes and intercepts for linear regressions relating
n to Tth at T a values of 13, 20 and 25°C were indistinguishable from the relationship
describing all data regardless of T a . Furthermore, frequency data were similar to
those we presented previously (Casey et al. 1981).
Instantaneous oxygen consumption
As in the study of Bartholomew et al. (1981), changes in Ttj, during warm-up
reflect changes in oxygen consumption. A slight curvilinearity occurred in the rate of
oxygen uptake which was not reflected in the change in Tth. Fig. 2 shows a typical
polygraph trace of oxygen consumption at T a = 25°C. Despite the design of our
system, this curvilinear change of apparent fractional oxygen concentration of excurrent air ( F E O ) with time appears to be an artifact due to time lags and rapid rates
of change of oxygen uptake (Bartholomew et al. 1981). The difference between
apparent and actual instantaneous FEQ was always greatest at high T a and was much
less pronounced or completely absent at low T a . After appropriate correction
had been applied, all V o data, regardless of T a , increased linearly with time.
Energetics and muscle performance
393
Rates of heat production during warm-up are directly related to thoracic
temperature, varying from about 10mW at T ^ of 15°C to 75 mW at T th of 40°C
(Fig. 3). HP was dependent only on T ^ . Thus, a moth warming at T a of 13 or 25°C
had an instantaneous rate of heat production of approximately 45 mW at T ^ of 30°C.
These values are similar to predictions based on heat exchange analyses in their linear
relationship to Tth and their independence of T a , but are substantially greater in
magnitude.
J? 0-2085
0-2087
19
Fig. 2. Strip chart recording showing the apparent fractional oxygen concentration of
excurrent air (FEQ 2 ) and thoracic temperature (T t h) change during pre-flight warm-up
and post-flight cooling, T , = 25 °C.
80
60
3
O
40
OOO
D.
20
# •
15
20
25
30
35
Thoracic temperature (°C)
40
Fig. 3. The relationship of heat production to thoracic temperature at T a values of
13 ( • ) , 20 (•*•) and 25 (O)°C. Each point at any given T j , represents a separate
individual. Solid line indicates linear regression.
394
T. M. CASEY AND J. R. HEGEL-LITTLE
Since heat production is a function of thoracic temperature and independent of T a
(Fig. 3), while the rate of thoracic temperature increase is directly related to T a ,
the rate of change of the metabolic rate during warm-up should show a similar
dependence on ambient temperature. Metabolic rate increases continuously during
warm-up and the rate of increase is linearly related to T a (Fig. 4). There is good
correspondence between the rates of increase of metabolic rate and of T t h during
warm-up. Between T a values of 15 and 25°C, each parameter increases about three
times (Figs 1,4).
Cost of warm-up and cooling
Due to its very small mass (X = 90 mg), heat loss, and therefore T a , should have a
strong effect on the total cost of both warm-up and cooling inM. americanum. Fig. 5
illustrates the rates of energy expenditure during pre-flight warm-up and post-flight
cooling at ambient temperatures of 13 and 25 °C. At high T a , a moth has a higher
initial rate of heat production due to a higher muscle temperature. It also increases its
rate of heat production more rapidly because more of the heat is being used to warm
the thorax. Both of these factors reduce the duration of warm-up at the higher T a .
Indeed, over a 12°C range of T a , the duration of pre-flight warm-up varies almost
eight times (Fig. 5). Since the total cost of warm-up at each T a equals the area under
each of the trapezoids in Fig. 5, Ta is obviously a major determinant of the total cost
of warm-up in M. americanum, in sharp contrast to the situation in flight where
energy metabolism is independent of T a (Casey, 1981a).
The total energy expended during pre-flight warm-up and post-flight cooling is
shown in Fig. 6. Over the range of Ta from 13 to25°C, the cost of warm-up decreases
about five times. Such large differences are not apparent in the energetics of postflight cooling. There was a slight, significant difference between the total energy
expenditure during cooling at different T a values (1 -25 J vs 0-5 J, Fig. 6). Although
the energy expended during cooling is greater at the lower T a the relative increase
in the cost of warm-up is much greater. As a consequence, cooling represents only
about 5 % of the energetic episode at T a of 13°C compared with about 10% at T a of
25°C(Fig. 6).
Energetics and muscle performance
Metabolism during warm-up can increase as a result of an increase in n, an increase
in the energy expended per wing stroke (the stroke work input, E/M) or both. E/n
is considerably higher than previously calculated (Fig. 7) and at low thoracic
temperatures it is temperature-dependent. At T th greater than 25 °C, however, stroke
work input is essentially independent at about 1-1 mj. Thus, most of the increase of
energy metabolism as warm-up proceeds is mediated by increased frequency of
muscle contraction which occurs as a result of increased T t h. Measured values for
stroke work during warm-up are comparable to values obtained for M. americanung
during free hovering flight.
Energetics and muscle performance
395
DISCUSSION
Energetics
The rate of heat production is related to T t h ) but not to T a (Fig. 3). Since heat
loss is proportional to T th —T a , rate of thoracic temperature increase is strongly
^
I
30
c
'i
11
20
10
10
30
20
Ambient temperature
Fig. 4. The rate of change of metabolic rate during warm-up in relation to ambient
temperature. Horizontal lines represent mean values ±S.D., numbers indicate sample
size. Diagonal line represents linear regression.
0
1
2
3
4
5
6
Time (min)
7
8
9
Fig. 5. Energy expenditure of Malacosoma americanum during pre-flight warm-up and
post-flight cooling at T , values of 13 and 25°C.
396
T. M. CASEY AND J. R. HEGEL-LITTLE
20
Instantaneous
1
15
i.
X
u
S3 10
10
20
15
25
30
Fig. 6. Total energy expenditure (J) during pre-flight warm-up (•) and post-flight
cooling (+) at different ambient temperatures. Data are obtained by integrating the area
under the curve for instantaneous VQZ versus time during warm-up and cooling.
2-0 r
Measured
1 1-0
Calculated
10
15
20
25
30
35
40
45
Thoracic temperature (°C)
F i g . 7. T h e relationship of energy expenditure per wing stroke work input (E/rc) to
thoracic t e m p e r a t u r e . Data for Malacosoma amencanum
during free hovering flight are
from Casey (1981). Calculated data represent estimates for M. amencanum
based on
thoracic heat storage and heat loss (Casey, Hegel & Buser, 1981).
Energetics and muscle performance
397
dependent on T a . Similarly, rate of change of heat production (mWmin"1) is also
strongly related to T a (Fig. 4). While metabolic data from the present study agree
qualitatively with previous understandings of the energetics of warm-up (Heinrich &
Bartholomew, 1971; Heinrich, 1975; May, 1979; Casey et al. 1981; Hegel & Casey,
1982), the magnitude of heat production is much greater than previous estimates for
M. americanum (Casey et al. 1981) because they were based solely on heat storage
and heat loss in the thorax, and did not include the head, abdomen or respiratory
system as additional avenues of heat exchange. Measured rates of heat exchange from
the head and abdomen of the sphingid Manduca sexta accounted for about 24—27 %
at T a values from 16 to 30°C (Hegel & Casey, 1982). Data reported by Bartholomew
et al. (1981) also indicate a significant difference between measured VQ values and
heat exchange values.
Cost of warm-up and cooling
Our data suggest that the energetic cost of cooling is a very small fraction of the
total cost of warm-up at all T a values (Fig. 6). These results are in marked contrast to
those of Bartholomew et al. (1981), who report that the cost of cooling amounts to
69—75 % of the cost of warm-up. The sphingids and saturniids spend substantially
more time in cooling than in warm-up (Bartholomew et al. 1981, their figs 2, 3, 4).
The small size and high thoracic conductance of M. americanum compared with that
of sphingids and saturniids is probably responsible for much of this discrepancy.
Due to these factors, the cost of elevating T ^ is very high and high levels of heat loss
reduce the effectiveness of heat storage, thereby increasing the total duration (and
therefore the total cost) of warm-up, particularly at low T a . However, the same
factors facilitate rapid post-flight cooling. Consequently, M. americanum achieves
resting thermal states much more rapidly than larger moths, which reduces its total
cost of cooling.
Our data indicate that heat production by Malacosoma is considerably greater than
was previously reported but they do not necessarily indicate that this represents a
maximal effort. A strong selective pressure for maximal output during warm-up
based on predator avoidance has routinely been presented (see Introduction) and our
data are consistent with that interpretation. However, perhaps a more compelling
argument applies for M. americanum because these moths routinely fly during early
morning hours when T a is 15°C or less (Casey, 1981a). At this temperature, cost of
warm-up is very high due to the low rate of thoracic temperature increase and
consequent long time required to reach flight temperature (Fig. 5). If the moth could
increase metabolic rate above measured levels (polygon C in Fig. 8A) it could
substantially reduce the time necessary for warm-up. Since there is a steep inverse relationship between total cost of warm-up and the rate of warm-up (Fig. 8B),
small changes in the latter would result in substantial reductions in the cost of warmup at ecologically relevant air temperatures. Thus, under most conditions warming
as rapidly as possible is cheaper than warming at a slower rate.
It is clear that T a is ah important determinant of the energetics of warm-up. In the
sphingid, M. sexta, a drop in T a from 30 to 16°C triples the cost of warm-up (Hegel
398
T. M. CASEY AND J. R. HEGEL-LITTLE
20 - B
• C
r
A
15 -
\
10
^ » A
5 -
4
6
Time (min)
5
i
i
i
10
15
20
AE/At (mWmin" 1 )
Fig. 8. (A) Energy metabolism in relation to time for a hypothetical moth at T . of 15°C
assuming different rates of increase of metabolism. Polygon C represents the measured
value. (B) Total cost of warm-up obtained by integrating the polygons in Fig. 8A as a
function of the rate of increase of metabolism (AE/At).
& Casey, 1982). Our data indicate that thermal effects are even greater for smaller
moths (Figs 6, 8). Consequently, scaling estimates of the energetics of warm-up
(Bartholomew & Casey, 1978; Bartholomew et al. 1981) are difficult to evaluate
when based on a single T a value. Conclusions based on such data should be made
with care due to the large numbers of variables involved, strong interactions between
T t h and n for moths of different morphology (Kammer & Heinrich, 1978; Casey
et al. 1981) and between various conductances (head, thorax, abdomen) with mass,
T a and insulation (Hegel & Casey, 1982). Comparative data on Vo during warm-up
similar to those obtained by Bartholomew et al. (1981) for moths of different sizes at
low T a would be extremely useful, as would studies of muscle frequency vs T t h for
moths differing in size and wing morphology.
Muscle energetics and performance
It is generally assumed that mechanical power requirements and metabolic rate
should be closely related during flight (Weis-Fogh & Alexander, 1977; Casey, 1981;
Ellington, 1985). During warm-up, however, it should be adaptive to convert as
much of the expended energy into heat as possible (i.e. be very inefficient) to
minimize the duration and the cost of warm-up. For insects, as well as for ectothermic vertebrates, muscle performance is very temperature-sensitive (Josephson,
1981; Bennett, 1985) and much of the thermal sensitivity is associated with temporal
characteristics of muscles while tension development appears to be relatively insensitive. These characteristics are consistent with our data for energy expenditure
M. americanum during warm-up. Most change in energy expenditure results fro
Energetics and muscle performance
399
change in contraction frequency while change in E/M is relatively insensitive to
temperature (Fig. 7).
The frequencies of muscle contraction during warm-up and flight are comparable
in M. americanum at the same T ^ . Since the energy expended per muscle
contraction is also similar whether the animal is warming up or flying, our data
suggest a comparable neural input to the muscles during each activity. Obviously,
the change in muscle function in the transition from warm-up to flight (providing lift
and aerodynamic power) need not require different energy expenditure. Change in
mechanical power output can be accomplished by a change in the phase of contraction between the elevators and depressors (Kammer, 1968). During warm-up the
muscles are contracting almost simultaneously so that virtually all the energy is
degraded to heat as the muscles work against each other. By contracting alternately
each muscle set can do useful work on the surrounding air. Thus, change in muscle
function between warm-up and flight at the same thoracic temperature represents a
change in muscle efficiency which is consistent with the functions they serve in each
activity. The moths must retain the capacity for additional increases in power during
flight to accommodate sudden aerobatic manoeuvres and climbing flight. Double
firing of the motor neurones innervating the flight muscle (Wilson & Weis-Fogh,
1962; Kammer & Heinrich, 1978) would allow for increased power output by
increasing frequency and stroke amplitude (Kammer & Rheuben, 1981).
Results from the present study are very similar to those obtained for bumble-bees,
which also show equivalent muscle metabolism per action potential at a given Tth,
regardless of whether they are in warm-up or flight (Kammer & Heinrich, 1974).
While synchronous and asynchronous fliers may differ in muscle morphology and
physiology (Ellington, 1985), motor patterns (Kammer & Rheuben, 1981) and in
the magnitude of energy expended per muscle contraction (Casey, May & Morgan,
1985), they show comparable responses to temperature and similar patterns of
muscle energetics in the transition from warm-up to flight. For M. americanum as
well as for the bees, the limitation to take-off is a thermal dependence of muscle
contraction frequency. Once T,h is elevated to a sufficient level for the muscles to
operate at appropriate wing stroke frequencies flight commences.
We are pleased to thank Drs W. A. Buttemer, C. P. Ellington, B. A. Joos, M. L.
May and R. D. Stevenson for stimulating and illuminating discussions. Supported
by NSF grant PCM8219311 and by the New Jersey State Experiment Station
(Project 08511).
REFERENCES
BARTHOLOMEW, G. A. & CASEY, T . M. (1978). Oxygen consumption of moths during rest, preflight warm-up, and flight in relation to body size. J. exp. Biol. 76, 11-25.
BARTHOLOMEW, G. A. & HEINRICH, B. (1973). A field study of flight temperatures in moths in
relation to body weight and wing loading..7. exp. Biol. 58, 123-135.
BARTHOLOMEW, G. A., VLECK, D. & VLECK, C. M. (1981). Instantaneous measurements of oxygen
consumption during pre-flight warm-up and post-flight cooling in sphingid and saturniid moths.
J. exp. Biol. 90, 17-32.
400
T. M. CASEY AND J. R. HEGEL-LITTLE
BENNETT, A. F. (1985). Temperature and muscle. J . exp. Biol. 115, 333-344.
CASEY, T. M. (1981). Energetics and thermoregulation of Malacosoma
amencanum
(Lepidoptera: Lasiocampidae) during hovering flight. Physiol. Zool. 54, 362-371.
CASEY, T. M., HEGEL, J. R. & BUSER, C. S.(1981). Physiology and energetics of pre-flight warmup in the eastern tent caterpillar moth, Malacosoma americanum.J. exp. Biol. 94, 119-135.
CASEY, T. M., MAY, M. L. & MORGAN, K. R. (1985). Flight energetics of euglossine bees in
relation to morphology and wing stroke frequency. J. exp. Biol. 116, 271-289.
DOTTERWEIGH, H. (1928). Beitrage zur Nervenphysiologie der Insekten. Zool. Jb. (Physiol.) 44,
399-450.
ELLINGTON, C. P. (1985). Power and efficiency of insect flight muscle. J . exp. Biol. 115, 293-306.
HEGEL, J. R. & CASEY, T . M. (1982). Thermoregulation and control of head temperature in the
sphinx moth, Manduca sexta.J. exp. Biol. 101, 1—15.
HEINRICH, B. (1974). Thermoregulation in endothermic insects. Science 185, 747-756.
HErNRiCH, B. (1975). Thermoregulation in bumblebees. II. Energetics of warm-up and free flight.
J. comp. Physiol. 96, 155-166.
HEINRICH, B. & BARTHOLOMEW, G. A. (1971). An analysis of pre-flight warm-up in the sphinx
moth, Manduca sexta.J. exp. Biol. 55, 223-239.
HEINRICH, B. & CASEY, T. M. (1973). Metabolic rate and endothermy in sphinx moths. J. comp.
Physiol. 83, 195-206.
HEINRICH, B. &MOMMSEN, T. P. (1985). Flight of winter moths near 0°C. Science 228, 177-179.
Joos, B. A. (1986). Biochemical correlates of pre-flight warm-up in the sphinx moth, Manduca
sexta. Doctoral dissertation, University of Michigan, Ann Arbor. 95pp.
JOSEPHSON, R. K. (1981). Temperature and mechanical performance of insect muscle. In Insect
Thermoregulation (ed. B. Heinrich), pp. 19-44. New York: Wiley.
KAMMER, A. E. (1968). Motor patterns during flight and warm-up in Lepidoptera. J. exp. Biol. 48,
89-109.
KAMMER, A. E. (1981). Physiological mechanisms of thermoregulation. In Insect Thermoregulation (ed. B. Heinrich), pp. 115-158. New York: Wiley.
KAMMER, A. E. & HEINRICH, B. (1974). Metabolic rates related to muscle activity in bumblebees.
J. exp. Biol. 61, 219-227.
KAMMER, A. E. & HEINRICH, B. (1978). Insect flight metabolism. Adv. Insect Physiol. 13,
133-288.
KAMMER, A. E. & RHEUBEN, M. B. (1981). Neuromuscular mechanisms of insect flight. In
Locomotion and Energetics in Arthropods (ed. C. F. Herreid, II & C. R. Fourtner), pp.
163-194. New York: Plenum Press.
KROGH, A. & ZEUTHEN, E. (1941). The mechanism of flight preparation in some insects. J. exp.
Biol. 18, 1-10.
MAY, M. L. (1979). Energy metabolism of dragonflies (Odonata: Anisoptera) at rest and during
endothermic warm-up. .7. exp. Biol. 83, 79-94.
WEIS-FOGH, T. & ALEXANDER, R. MCN. (1977). The sustained power output from striated
muscle. In Scale Effects in Animal Locomotion (ed. T. J. Pedley), pp. 511-525. Town:
Publisher.
WILSON, P. M. & WEIS-FOGH, T. (1962). Patterned activity of coordinated motor units, studied in
flying locusts. J . exp. Biol. 39, 643-667.